Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
RESEARCH ARTICLE
Open Access
Consistent phenological shifts in the making of
a biodiversity hotspot: the Cape flora
Ben H Warren1,15*, Freek T Bakker2, Dirk U Bellstedt3, Benny Bytebier3,16, Regine Claßen-Bockhoff4,
Léanne L Dreyer5, Dawn Edwards6, Félix Forest7, Chloé Galley8, Christopher R Hardy9, H Peter Linder8,
A Muthama Muasya10, Klaus Mummenhoff11, Kenneth C Oberlander5, Marcus Quint4, James E Richardson12,
Vincent Savolainen7,13, Brian D Schrire14, Timotheüs van der Niet8,16, G Anthony Verboom10, Christopher Yesson1,
Julie A Hawkins1
Abstract
Background: The best documented survival responses of organisms to past climate change on short (glacialinterglacial) timescales are distributional shifts. Despite ample evidence on such timescales for local adaptations of
populations at specific sites, the long-term impacts of such changes on evolutionary significant units in response
to past climatic change have been little documented. Here we use phylogenies to reconstruct changes in
distribution and flowering ecology of the Cape flora - South Africa’s biodiversity hotspot - through a period of past
(Neogene and Quaternary) changes in the seasonality of rainfall over a timescale of several million years.
Results: Forty-three distributional and phenological shifts consistent with past climatic change occur across the
flora, and a comparable number of clades underwent adaptive changes in their flowering phenology (9 clades; half
of the clades investigated) as underwent distributional shifts (12 clades; two thirds of the clades investigated). Of
extant Cape angiosperm species, 14-41% have been contributed by lineages that show distributional shifts
consistent with past climate change, yet a similar proportion (14-55%) arose from lineages that shifted flowering
phenology.
Conclusions: Adaptive changes in ecology at the scale we uncover in the Cape and consistent with past climatic
change have not been documented for other floras. Shifts in climate tolerance appear to have been more
important in this flora than is currently appreciated, and lineages that underwent such shifts went on to contribute
a high proportion of the flora’s extant species diversity. That shifts in phenology, on an evolutionary timescale and
on such a scale, have not yet been detected for other floras is likely a result of the method used; shifts in
flowering phenology cannot be detected in the fossil record.
Background
Niche conservatism - the tendency of species to retain
ancestral limits in tolerances to environmental factors has a long history [1,2]. From a theoretical perspective,
it is supported by the expectation that rates of adaptation of populations to environments outside of the fundamental niche are slow relative to the time to
extinction in such environments [3-6]. These assertions
based on theory have been followed by a suite of
* Correspondence: ben.warren@cirad.fr
1
School of Biological Sciences, Lyle Tower, University of Reading,
Whiteknights, Reading RG6 6BX, UK
Full list of author information is available at the end of the article
empirical studies that have found evidence both for
niche conservatism [7-9] and against it [10-12]. In a
recent review, Wiens and Graham [13] conclude that
whether niches are conserved or not may simply depend
on how similar niches must be to be considered conserved, and that a more productive focus might be on
how well the concept of niche conservatism allows us to
predict outcomes in different areas of ecology and
evolution.
Here we use a phylogenetic approach to investigate
changes in distribution and flowering phenology of a
species-rich flora through a period in which it was
exposed to numerous climatic changes of a consistent
© 2011 Warren et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in
any medium, provided the original work is properly cited.
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
and repetitive nature, and compare how organisms that
responded in different ways have contributed to extant
species diversity. Our study uses phylogenies representing 20% of the extant angiosperm flora of the Cape of
South Africa (1800 of the 8900 species), a biodiversity
hotspot that has experienced climatic changes associated
with strong seasonal aridification since the Neogene (ca.
2-14 million years ago), likely in several different
episodes [14].
Elsewhere in the world, at an intra-specific level, a
plethora of past studies have found evidence for local
adaptation to contemporary climate change at specific
sites [15], although some dispute this evidence in all but
a minority of cases [16,17]. However at the level of species or evolutionarily significant units, the traditional
view is based on the fossil record [18-20], which shows
that in response to past climatic changes in the Quaternary (fluctuations occurring on the timescale of thousands of years, within the last 2.6 million years) species
underwent dramatic distributional shifts, but retained
remarkable stability in phenotype and inferred ecology.
The importance of distributional shifts on this timescale
is further supported by the success of ecological niche
models in predicting ancient distributions [21,22].
Over timescales of millions of years, the documented
response of floras to past environmental change is that
of species-level turnover [23,24]. It is likely that there is
a strong adaptive component to such turnover, but an
understanding of the relative roles of adaptation and
species sorting is complicated by the fact that the timescale of change (hundreds of thousands to millions of
years) corresponds to the typical duration of species;
many of the characters detected in the fossil record that
may exhibit adaptive responses to past climatic change
(e.g. leaf micromorphological features such as stomatal
density and distribution, and trichome abundance) are
themselves used for species delimitation. While flowering phenology is subject to strong physiological constraints and therefore likely to be strongly linked to
climate, it cannot be inferred from the fossil record,
regardless of timescale. Reconstructions based on molecular phylogenetic data offer certain advantages over the
fossil record with respect to these issues. Notably, the
characters used for lineage delimitation are different
from those used to detect adaptive responses to climate
change. Further, it is possible to include in an analysis
both a wide breadth of lineages, including those absent
from the fossil record, and any character identifiable
across their living representatives.
The species-rich Cape Floristic Region (CFR) provides
a model system in which to assess the utility of niche
conservatism in explaining floral responses to past climatic change. Firstly, the concentration of the Cape’s
floral species diversity within a small number of
Page 2 of 11
unusually large endemic or near-endemic radiations permits the development of robust phylogenetic hypotheses
through intense sampling focused in a small geographic
area. Consequently, molecular phylogenetic coverage of
plant lineages in this biota is more complete than that
of any other biodiversity hotspot. Secondly, despite
being unusually species-rich both for its area and latitude, the entire seed-plant flora has been catalogued,
with detailed locality and phenological information
available for each species [25]. Thirdly, the CFR spans
two regions with a major difference in climatic regime
(Figure 1). The eastern region has a nonseasonal rainfall
climate, while the western region has a strictly winter
rainfall (Mediterranean-type) climate. Evidence from
global climate data support a nonseasonal rainfall climate across the Cape in the Early-Mid Miocene [26,27].
This was followed by a seasonal aridification trend along
the west coast [14], the precise timing of which is
uncertain, in which summer rainfall was reduced and
winter rainfall was increased. Evidence from fossil data
supports numerous later fluctuations between nonseasonal rainfall and winter rainfall regimes in the western
region, culminating in the modern winter rainfall regime
in the western region [28-34]. However the number and
precise timing of these fluctuations remain uncertain.
The current flora of the winter rainfall region shows
a peak of flowering in the spring (September-October),
while that of the nonseasonal rainfall region shows a
peak in late-spring/early summer (October-November)
[35]. Species in the winter rainfall region also show a
shorter mean duration of flowering (3.21 months, n =
3670 for all seed plant species; 3.05 months, n = 877
for all species in clades sampled) than species confined
to the east (4.04 months, n = 2316 for all seed plant
species; 3.56 months, n = 373 for all species in clades
sampled; [25]). These two patterns are consistent with
expectations if insufficient moisture for physiological
activity is the main factor limiting summer flowering
in the CFR [35]. Species occupying the Cape-wide nonseasonal rainfall regime prior to the summer aridification trend, and that were physiologically vulnerable to
the new climate, could have survived by adapting to
the new climate, by changing their distribution, or a
combination of the two. Based on the broad pattern of
aridification since the Mid Miocene, the predicted
direction of adaptive changes in phenology would be
from long-duration summer flowering to shorterduration spring flowering. This predicted directionality
holds regardless of whether adaptive changes are the
result of fixed genetic changes or plastic responses. In
terms of distribution, reduced survival in the west, and
distributional shifts towards the east where the effects
of summer aridification were less severe, would also be
predicted.
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
Page 3 of 11
Figure 1 Location of the Cape Floristic Region in southern Africa as defined by Goldblatt & Manning [25]. Western and eastern regions
with winter and nonseasonal rainfall regimes, respectively, are indicated, along with representative seasonal rainfall charts (after [84]).
We compiled molecular phylogenies representing 20%
of the angiosperm species diversity of the CFR [36-50]
as defined by Goldblatt and Manning [25]. These 18
molecular phylogenies represent monophyletic floral
clades largely or entirely restricted to the Cape, estimated to have diversified within the last 46 Myr
[39,40,42,45,47,48,50-55]. Published data [25] for geographical distributions and for the timing and duration of
flowering of extant species were used to reconstruct
maximum likelihood (ML) estimates of the ancestral
states of these clades.
Our aim was to test the relative contribution of distributional shifts and adaptive change in the response of
the Cape flora to climatic changes since the midMiocene. If niche conservatism predominates, then
lineages must track the non-seasonal rainfall regime from
the West to the East in order to continue to occupy a physiologically favourable environment. We therefore expect
lineages whose ancestors experienced climate change in
the West to show distributional shifts to the East.
A species’ niche is the multidimensional set of biotic
and abiotic conditions in which it is able to persist and
maintain stable population sizes. For a flowering plant,
one aspect of its overall niche is its flowering phenology i.e. the timing and duration of its flowering period. Since
flowering is known to be limited physiologically by many
aspects of climate [56], we consider flowering phenology
to be one of the suitable dimensions of niche space in
which to look for adaptive shifts in response to past
changes in climate in the Cape. Adaptive changes in
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
phenology could considerably modify species climate
envelopes, but not necessarily accompany a shift of
biome or vegetation type. Whether adaptive changes
result from fixed genetic changes or plastic responses is
best determined by experimental transplantation of
plants, which has not yet been carried out in the Cape.
These two mechanisms cannot be distinguished on the
basis of phylogeny alone. Nonetheless, the identification
of the scale of such changes using phylogeny can serve
as a stimulus for future experimental work. In screening
the Cape flora for changes consistent with predictions
under past seasonal aridification, we find a number of
distributional shifts. Surprisingly however, shifts in flowering phenology of lineages consistent with predictions
also occur, are similar in frequency to distributional
shifts, and belong to lineages that have proceeded to
contribute a large proportion of species-diversity to the
extant flora.
Results
Our phylogenetic reconstructions demonstrate that 9
clades have undergone shifts in flowering pattern consistent with predictions based on past climate change
(Figure 2; Table 1). How the number of shifts per Cape
clade are counted depends on the treatment of nodes
for which character states are unresolved; we use the
basal-most possible position of shifts (as in additional
file 1: AF1.pdf) in order to produce figures that are
comparable across Cape clades. On this basis, shifts in
flowering pattern consistent with predictions consist of
one (Figure 2, and see AF1.pdf, Trees 5, 8, 10, 12 &13),
two (AF1.pdf, Tree 6) or four (AF1.pdf, Tree 5) shifts in
flowering duration per Cape clade, and one (AF1.pdf,
Trees 3, 5, 6 & 9) or two (AF1.pdf, Tree 5) shifts in the
timing of flowering per Cape clade, making a total of
eleven shifts in flowering duration and six shifts in the
timing of flowering detected across the sampled flora.
By contrast, four clades have undergone shifts in flowering pattern contrary to predictions (Table 1, additional
file 2: AF2.pdf); these consist of one (AF1.pdf, Trees 5 &
10) and two (AF1.pdf, Tree 14) shifts in flowering duration per Cape clade, and one shift in the timing of flowering per Cape clade (AF1.pdf, Trees 5, 10 & 12),
making a total of four shifts in flowering duration and
three shifts in the timing of flowering contrary to predictions detected across the flora.
In terms of distribution, 12 clades show predicted
shifts from the west towards the east (intra-Cape shifts
out of the west, into the east, or a combination of the
two; Figure 2, Table 1); these consisted of one (AF1.pdf,
Trees 2, 10 & 13), two (Figure 2; AF1.pdf, Trees 1, 3,
7, 8, 9 & 12), three (AF1.pdf, Tree 5) and seven (AF1.pdf,
Tree 14) shifts out of the west and/or into the east per
Cape clade, making a total of 26 shifts in distribution
Page 4 of 11
detected across the sampled flora. By contrast, four
clades show distributional shifts from the east towards
the west, contrary to predictions (intra-Cape shifts out of
the east, into the west, or a combination of the two;
Table 1, AF2.pdf); in all cases these consisted of just one
(AF1.pdf, Trees 2, 5, 10 & 11) shift out of the west or
into the east per Cape clade, making a total of four shifts
in distribution contrary to predictions detected across
the flora.
Thus, of the 18 clades sampled in our study, almost as
many clades show shifts in flowering phenology consistent with adaptation to climate change (9 clades) as
show changes in distribution (12 clades). Seven clades
showed shifts in both phenology and distribution consistent with predictions. A smaller number of clades show
shifts in flowering phenology and distribution contrary
to adaptation to climate change (4 clades in each case,
of which two show both reverse patterns).
We also counted the number of Cape species in clades
that speciated following phenological and distributional
shifts, in order to determine the scale of contribution of
such lineages to the extant flora. When species numbers
in our sample are considered, and errors caused by
unsampled species and uncertainty in the exact node of
character state transition are allowed for, 14-55% of species belong to lineages that have experienced a shift in
phenology consistent with an adaptation to climate
change. By comparison, our reconstructions indicate
that 14-41% of species have arisen from ancestors that
showed a distributional shift consistent with climate
change.
Discussion
The reproductive output of plants depends on the finetuning of flowering to fit abiotic and biotic conditions
[57,58]. Thus flowering phenology has strong fitness
consequences, and flowering time is one factor determining a species’ niche [59]. Like other characters specifying a species’ niche, physiological or morphological,
flowering phenology may be conserved, plastic or
undergo evolutionary change [57,59].
It is well established that many plant populations can
and have changed their flowering time in the last century. Shifts in flowering phenology provide some of the
most compelling evidence that species are being influenced by contemporary global environmental change
[60-62]. These tracking responses, perceived as adaptations to changing environmental conditions, may be
environmentally induced plastic responses or evolutionary adaptations. Although genetic data is not available
for most of the species showing phenological responses
to climate change [17], there are several studies which
have demonstrated that responses can be heritable.
These include examples of crop plants responding to
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
Page 5 of 11
Figure 2 Phylogeny of Moraea showing reconstructed shifts in flowering duration and distribution under an ML model. All species are
in the genus Moraea except where otherwise indicated. Coloured balls at terminals indicate the flowering duration of species, while equivalent
coloured pie diagrams at each internal node depict the proportional likelihood for different flowering durations. One month, white; 2 months,
blue; 3 months, red; 4 months, green; 8 months, black. Nodes reaching the threshold of two log-likelihood units separating the flowering
duration of highest likelihood from alternative flowering durations are marked with an asterisk. Bars attached to the left side of nodes indicate
significant support (two log-likelihood units separation) for a reconstructed presence in the west; those to the right side of nodes indicate
significant support for a reconstructed presence in the east. Internal nodes with no horizontal bars are those for which the reconstructed
distribution is not significantly supported. A vertical bar below a node indicates 80-100% bootstrap support; a bar above the node indicates
50-79% bootstrap support; no vertical bar indicates 0-49% bootstrap support.
environmental changes in situ and invasive plants or
domesticates encountering new climate regimes as they
expand their distribution [63-67]. Differential tracking of
contemporary climate change has been shown to be a
determinant of the species composition of a community,
since populations of species lacking a plastic or microevolutionary response are locally extirpated [68,69].
These findings raise questions about the significance of
phenological adaptation to past climate change, since
the extent to which differential tracking of past climate
has shaped a whole flora is at present unknown.
Our study has identified a footprint of past phenological change, set in motion over five million years ago, in
a contemporary flora. A point that remains clear regardless of the relative roles of evolutionary changes and
phenotypic plasticity is that the observed phenological
shifts have had a major role in shaping the extant Cape
angiosperm flora; lineages that underwent shifts in
flowering phenology later speciated extensively. Our
study also provides tentative evidence of differential
tracking of climate change, with phenological shifts
apparent in some clades but not others.
The comparable number of shifts - distributional and
phenological - experienced by the Cape flora as a new
climate regime was established is a noteworthy finding
of our study. Table 1 shows that phenological shifts are
apparent in some clades (Crotalarieae, Disa, Heliophila,
Moraea, Muraltia, Oxalis, Pentaschistis, Phylica and
Podalyrieae) but not others. We go beyond estimation
of the frequency of shifts to estimate the scale of the
contribution these shifts have made to the character of
the present-day flora. While our confidence intervals are
wide - 14-41% and 14-55% of species belonging to
lineages that have experienced distributional and phenological shifts consistent with past climate change,
respectively - these figures indicate that contrary to
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
Page 6 of 11
Table 1 Phenological and distributional patterns in the eighteen Cape clades sampled
Cape Clade
Shift in flowering midpoint Shift in flowering duration Shift in distribution Date estimate (Ma) and method(s) used
Bruniaceae
Crotalarieae
✓1
Disa
✓
✓
b
✓
6.7-4 clock [55]
✓b
40-8.8 NPRS, multidivtime [39,52]
✓
27-1 multidivtime [53]
Ehrharta
Ficinia
Heliophila
✓
✓
Moraea
Muraltia
✓
Oxalis
3
✓
11-5.5 PL [85]
✓
✓
14-4 NPRS [42]
✓b
✓
Cape Restionaceae
b
2
5
Phylica
Podalyrieae
12.7-0.9 multidivtime [40]
✓
Pelargonium
Pentaschistis
5.8-1.0 NPRS, clock [45]
✓
Indigofera
✓
✓
✓
✓
✓
4
8-2 NPRS [47]
40-10 NPRS, multidivtime [39,52]
✓
✓
42-1.25 NPRS, clock [54]
Satyrium
Tetraria
✓b
Zygophyllum
For each Cape clade in question, ticks (✓) indicate one or more supported shifts in character state consistent with our past climatic change predictions. Unless
otherwise indicated, shifts in flowering midpoint are from the summer towards the spring, shifts in flowering duration are reductions in the number of months of
flowering, and shifts in distribution are out of the west and/or into the east. Where available, ranges of published date estimates for the shifts are listed, along
with the dating methods included in this range and reference to source publications.
✓b, clades in which some degree of later backward shifting is exhibited at the distal-most nodes. ✓1, in the Crotalarieae, the flowering midpoint is reconstructed
as shifting from summer to early spring deep within the Cape clade, followed by a much shallower shift to late spring and finally back to early spring. A
reduction in flowering duration is reconstructed both deep within the Cape clade, and towards the tips. 2, Pelargonium exhibits a shift from east to west at a
single distal-most node. 3, Oxalis exhibits a shift in reconstructed flowering midpoint from mid-May to the May-June boundary and/or to mid-June (i.e. from lateautumn slightly towards the winter). 4, the Cape Restionaceae exhibits a shift in reconstructed flowering duration from one to two months, and from one to five
months at a single distal-most node. In the only instance where such shifts do not involve very shallow nodes, a later shift back to one flowering month is
observed. 5, Depending on the nodes considered either side of those for which states are undetermined, Pentaschistis either exhibits a very slight shift in
flowering midpoint from summer towards the spring, or an equally slight shift from spring towards the summer.
certain schools of thought [18,20], adaptive changes
consistent with past climate change have had a significant impact on the Cape flora on the timescale considered (Early-Mid Miocene to the present). Such
adaptations may be close contenders to (often co-occurring)
distributional shifts in their frequency and contribution
to the modern flora. Our results, while suggestive of evolutionary changes, do not allow us to rule out a major
role for plasticity in the phenotypic adaptations that we
observe. Furthermore, flowering phenology is just one of
many important niche parameters of Cape plants, most
of which are presumably highly conserved, otherwise
there would not be large clades restricted to the Cape
(Cape clades), and the Cape Floristic Region as we know
it would not exist. Nonetheless, the patterns uncovered
demonstrate that both adaptive and distributional shifts
consistent with past climatic change have had strong
impacts on the assembly of this biodiversity hotspot,
since lineages that underwent these changes went on to
contribute a high proportion of its current species
richness.
While most of the observed shifts in distribution and
flowering patterns are consistent with predictions based
on past climate change, alternative explanations must be
considered. First, we consider the possibility that reconstructed shifts in flowering patterns result from changes
in distribution within the Cape, with a consequent phenological response to regions with differing climates,
rather than climatic change itself. This scenario can be
rejected because reconstructed shifts in flowering
pattern (long-duration summer flowering to shorterduration spring flowering) work in the opposite direction to predictions on the basis of reconstructed west to
east shifts in geography.
Second, we consider the possibility that reconstructed
shifts are an artefact of regional differences in species
diversity within the Cape; the west is known to harbour
higher species diversity than the east [14]. Were the
flowering duration or season of Cape species distributed
at random with respect to phylogeny, we might expect
the predominant flowering states observed in the west
(short-duration spring flowering) to be more frequently
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
reconstructed at the base of Cape clades than those
observed in the east (longer-duration summer flowering), purely as a result of them being the most frequent
in the dataset. This second scenario can be rejected,
since observed shifts in flowering phenology run in the
opposite direction to those predicted as a result of the
proposed diversity difference artefact.
Third, we consider the possibility that the patterns we
observe have arisen by chance. Our character randomizations of flowering midpoint across trees showing the
basal-most (Podalyrieae) and distal-most (Disa) shifts in
flowering midpoint showed that the probability of patterns consistent with past climatic change occurring by
chance are P = 0.00 and P = 0.1 respectively. If we take
the higher of these two probabilities as representative of
the maximal probability of shifts consistent with past
climatic change occurring by chance in any particular
Cape clade, and consider the five out of 18 Cape clades
for which shifts consistent with past climatic change
arose in the real data, we can reject the hypothesis that
the observed shifts occurred by chance (P = 0.0218).
It is appealing to link environmental changes and
shifts in phylogenies through estimations of the timescales on which they occurred. In the case of the seasonal aridification trend in the Cape flora, problems with
such an approach arise. The most significant of these is
the absence of data concerning the precise timing, frequency and nature of the aridification trends; much
more palaeobotanical and geological evidence is needed
if we are to narrow down their timing reliably within
the broad bounds of the Neogene. Notwithstanding this
caveat, in all sampled Cape floral clades for which date
estimates are available, confidence intervals for the timing of distributional and phenological shifts strongly
overlap with temporal bounds of the aridification event
(Table 1).
Since our phylogenies only sample living species, we
are unable to speculate on any responses of non-surviving lineages of the early flora prior to their extinction.
Clearly however, our conclusions regarding the type of
response of lineages that survived past climatic change
are unaffected by the type of response (or lack of
response) of lineages that became extinct. Further to
complete extinction, two patterns of local (regional)
extinction may be envisaged. The first is extinction
within the CFR with the lineage surviving as a “nonCape relative” outside the CFR; we refer to this as ‘Cape
departure’. The second is relatively rapid back-and-forth
shifting of distribution, leaving no significant distributional change between start and finish; we refer to this
as ‘back-and-forth shifting’.
Cape departure seems unlikely to present a major distortion of the broad-scale pattern presented here; such
cases are infrequent judging by the small number of
Page 7 of 11
complete departures from the CFR occurring within the
monophyletic (or nearly so) groups of Cape species
(‘Cape floral clades’). Therefore compared with most
continental floras, the CFR can be viewed as being close
to a closed system. Under the back-and-forth shifting
scenario, a lineage’s temporary absence accompanied by
a shift in phenology and reinvasion of the CFR could
have been misinterpreted as in situ phenological change.
However, we have to invoke local extinction in the Cape
at the time that the lineage colonized the neighbouring
region, followed by local extinction in that neighbouring
region as the lineage re-colonized the Cape. While this
is not impossible it should first be noted that virtually
any interpretation of a phylogeny can be refuted if
enough extinction events in the right place are hypothesised. The more extinction events that are needed, and
the more specific the placement of the extinct species
required, the less strong such counter-arguments may
seem. Here we require a minimum of two for each Cape
clade inferred to undergo a phenological shift, making
18 local extinction events in total. More importantly,
this scenario still involves phenological shifts. The only
difference is that the phenological shifts occur while the
lineages are outside the Cape, rather than being in situ.
This would be an important detail to note were evidence found in favour. However, our main conclusion that a large proportion of Cape clades have undergone
phenological shifts during a period of past climatic
change - would remain unchanged.
The cases of phenological shifts that we document
provide a highly conservative estimate of the likely frequency of niche shifts in the Cape flora overall; we
investigated shifts in timing and duration of flowering
only, and there are many other pathways by which
plants may have survived summer aridification events.
These include the evolution of an annual life form, and
changes in leaf longevity, sclerophylly, leaf size, root
depth and root storage, all of which are interpreted by
plant physiologists as mechanisms of drought resistance
[70-74]. Improvements in a species’ capability to survive
a higher incidence of fire [14] through resprouting or
reseeding may also have been important. While many of
these species traits might be ideal for testing for adaptation to aridification between closely related species, few
if any of them are likely to have been as important
responses across the taxonomic breadth of the Cape
flora as is flowering phenology.
Conclusions
Adaptive changes in ecology at this scale and consistent
with past climate change have not been documented for
other floras. For example, palynological studies, most
complete for the Northern hemisphere, suggest that
many plant species underwent major distributional shifts
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
in response to Late Quaternary climatic fluctuations but
appear to have remained unchanged in phenotype
[18,20]. The same applies to beetles [19]. Clearly however, such studies compare the external morphology of
living and fossil forms; on this basis, nothing can be
inferred about the stability or otherwise of characteristics such as phenology over this timescale.
Despite concordance with conclusions based on the
Quaternary fossil record (short timescales of 103 to 104
years), the phenomenon of niche conservatism initially
came as a surprise and paradigm shift to those familiar
with strong patterns of adaptive change in response to
biotic and abiotic changes over long timescales in the
fossil record (104-109 years, e.g. [75]). Nonetheless, this
paradigm and associated distributional shifts gain support from several lines of inference, including the success of ecological niche models in predicting
geographical distributions, most notably in reciprocal
comparisons between the Last Glacial Maximum (based
on fossils) and the present [21,22]. Such studies have
provided a picture of species’ geographic distributions
tracking particular climatic regimes closely [76]. Ecological niche models involving climate have also shown
strength in predicting the geography of species invasions
in different geographical settings [77], and in predicting
distributions of sister species separated by several million years of independent evolution [8]. Finally, a wealth
of population genetic studies have supported the conclusion that species underwent distributional shifts in
response to past climate change [78,79].
In terms of adaptive responses, numerous ecological
studies provide evidence for intraspecific adaptation to
current and past (Late Quaternary) climate change at
specific sites, predominantly in the northern hemisphere
[64,78-80]. The absence of occurrence of novel phenotypes across a whole species or evolutionarily significant
unit through periods of past climate change [15], as
inferred from the Quaternary fossil record, has recently
been questioned from palaeoecological perspectives [81].
However it has remained unchallenged by phylogenetic
studies. Given the high frequency of Cape lineages that
underwent phenological responses consistent with past
seasonal aridification, and the difficulty of recovering
such shifts from the fossil record, it is conceivable that
such shifts in niche through periods of past climate
change have been more prevalent than is currently
appreciated. Further, the importance of shifts in ecology
[15], in addition to range shifts [18], in the Cape flora’s
response to past climatic changes may have been underestimated. In addition to the limitations of the fossil
record in preserving ecological shifts, such shifts may be
more easily detected at the species level over the course
of longer timescales (104-109 years, for which fossil data
is not available in all biomes) than shorter ones
Page 8 of 11
(10 3 years). Considering the ongoing accumulation of
molecular phylogenetic data worldwide, we hope that our
findings will stimulate comparable investigations across
other biomes for which the timing and nature of past climatic changes have been more precisely documented.
Methods
Species sampling
Phylogenies of 18 floral clades largely or exclusively
restricted to the Cape were compiled from existing publications [36-50]. These clades vary in the number of
Cape species they include, from 20 to an estimated 378
species, cumulatively totalling 20% of the flora’s species
diversity. Cape clades were identified following Linder’s
[14] criteria. Sampling of Cape species within these
clades varied from 100% to 10% per phylogeny. Tree
topologies used for analysis were either one of the most
parsimonious trees, or the Bayesian tree gaining highest
posterior probability, with the exception of five Cape
clades for which only a consensus tree was available
from the source publication.
Character scoring
Flowering duration and the midpoint of flowering season were treated as separate characters and scored for
each species based on Goldblatt & Manning’s [25] data
on flowering period in months. Flowering duration was
scored with 12 states corresponding to number of
months, and midpoint of flowering was scored with 24
states corresponding to mid-points that fall either midmonth or at the transition between two months. Three
species had a split flowering season unlikely to result
from a paucity of records, and their flowering durations
and midpoints were consequently scored as missing
data. Distributional data were available in the form of
presence or absence in each of six phytogeographic centres that Goldblatt & Manning [25] used to subdivide
the Cape. Given the proximity between the boundaries
of these centres and the division of Johnson’s [35] two
rainfall regions, we scored species as present or absent
from Goldblatt & Manning’s [25] western (NW, SW)
and eastern (KM, LB, AP, SE) phytogeographic centres,
corresponding to Johnson’s [35] winter rainfall and nonseasonal rainfall regimes respectively.
Reconstruction of ancestral states and state shifts
Ancestral states were reconstructed using a single-rate
maximum likelihood (ML) model implemented in Mesquite version 1.11 [82]. The advantage of this approach
is that it permits an estimate of the uncertainty in state
reconstruction [83]. A minimum of two log-likelihood
units separating a single state of highest likelihood from
alternative states was used as a threshold for determining the state optimisation of each internal node.
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
Optimisations at nodes for which this threshold is not
reached, or for which two log-likelihood units separate
more than one state of high likelihood from others, were
considered undetermined. Where nodes optimised as different states are separated by nodes in which the ancestral
state is undetermined, we quote species diversities under
the two extremes (deepest and shallowest) of potential
location of the state shift. Likewise, we quote species diversities of clades under the two extremes of placement of
unsampled species. To calculate the probability of shifts
consistent with past climatic change occurring by chance,
we carried out randomizations in which we permuted the
observed taxa among the terminal nodes in any given tree
using the Reshuffle Terminal Taxa option in the TreeFarm
package of Mesquite. Fifty randomizations of flowering
midpoints were conducted across two Cape clades selected
to represent trees with the basal-most and distal-most placement of flowering midpoint shifts. The resulting 100
trees were manually examined for shifts consistent with
past climatic change, following the same criteria that were
used in the observed data.
Additional material
Additional file 1: Molecular phylogenetic trees with reconstructed
shifts in geographic distribution and flowering patterns (flowering
durations and flowering midpoint) indicated. Unless otherwise
indicated, shifts in flowering patterns are in the direction consistent with
past climatic change; shifts in flowering midpoint are from the summer
towards the spring, and shifts in flowering duration are reductions in the
number of months of flowering. Where nodes optimised at different
states are separated by nodes in which the ancestral state is
undetermined, we have marked on the basal-most possible location of
the shift.
Additional file 2: Table illustrating the degree of shift in flowering
phenology in the eighteen Cape clades sampled. Mid-month
flowering midpoint character states are indicated by an abbreviation for
the month in question, while character states at the boundary between
two months are indicated by those two month abbreviations separated
by a hyphen. Flowering durations are in months. Shifts from the base of
the tree towards the tips are indicated as “>“. Note that all possible
series in the degrees of shift of flowering midpoint and duration are
listed. Many nodes optimised at different states are separated by nodes
for which the ancestral state is undetermined. Therefore, how many
shifts are counted depends on the criteria used to count them. In order
to be conservative in our counting, we have counted shifts in the text, in
Table 1 and in additional file AF1.pdf based on the basal-most possible
location of each shift. As a result of these criteria and tree shape, there
are many more possible series in the degrees of shifts marked here than
there are basal-most possible positions of shifts in the text, Table 1 and
file AF1.pdf.
Acknowledgements
We thank John Manning for supplying published data in electronic format
and three anonymous reviewers for constructive comments on the
manuscript. This work was funded by a grant from the Leverhulme Trust.
Author details
School of Biological Sciences, Lyle Tower, University of Reading,
Whiteknights, Reading RG6 6BX, UK. 2Biosystematics Group, Wageningen UR,
1
Page 9 of 11
& Nationaal Herbarium Nederland, Wageningen University branch, Generaal
Foulkesweg 37, 6703 BL Wageningen, The Netherlands. 3Department of
Biochemistry, Stellenbosch University, Private Bag X1, 7602 Matieland, South
Africa. 4Institut für Spezielle Botanik, Johannes Gutenberg-Universität Mainz,
Bentzelweg 2, 55099 Mainz, Germany. 5Department of Botany and Zoology,
Stellenbosch University, Private Bag X1, 7602 Matieland, South Africa. 6Royal
Horticultural Society Garden Wisley, Woking, Surrey, GU23 6QB, UK. 7Jodrell
Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK.
8
Institute for Systematic Botany, University of Zürich, Zollikerstrasse 107, CH
8008, Zürich, Switzerland. 9J.C. Parks Herbarium, Department of Biology,
Millersville University, Millersville, Pennsylvania 17551, USA. 10Department of
Botany, University of Cape Town, Private Bag X3, 7701 Rondebosch, South
Africa. 11University of Osnabrueck, Department of Biology/Botany,
Barbarastrasse 11, 49069 Osnabrück, Germany. 12The Royal Botanic Garden
Edinburgh, 20a Inverleith Row, Edinburgh EH3 5LR, UK. 13Imperial College
London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK. 14The Herbarium,
Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK. 15UMR C53
PVBMT, CIRAD-Université de la Réunion, 7 chemin de l’IRAT, Ligne Paradis,
97410 Saint Pierre, France. 16School of Biological and Conservation Sciences,
University of KwaZulu-Natal, Pr. Bag X01 Scottsville Pietermaritzburg 3209,
South Africa.
Authors’ contributions
BHW and JAH conceived and designed the study; FTB, DUB, BB, RC, LLD, DE,
FF, CG, CRH, HPL, AMM, KM, KCO, MQ, JER, VS, BDS, TV and GAV provided
phylogenetic data and feedback on results; CY reformatted phenological
and distributional data; BHW coordinated data assembly and conducted all
analyses; BHW and JAH wrote the manuscript; all authors edited and
approved the final manuscript.
Received: 7 September 2010 Accepted: 8 February 2011
Published: 8 February 2011
References
1. Grinnell J: The niche-relationship of the California thrasher. Auk 1917,
34:427-433.
2. Hutchinson GE: A Treatise on Limnology. New York: Wiley & Sons; 1957.
3. Kawecki TJ, Stearns SC: The evolution of life histories in spatially
heterogeneous environments - optimal reaction norms revisited.
Evolutionary Ecology 1993, 7(2):155-174.
4. Brown JS, Pavlovic NB: Evolution in heterogeneous environments - effects
of migration on habitat specialization. Evolutionary Ecology 1992,
6(5):360-382.
5. Holt RD, Gaines MS: Analysis of adaptation in heterogeneous landscapes
- implications for the evolution of fundamental niches. Evolutionary
Ecology 1992, 6(5):433-447.
6. Houston AI, McNamara JM: Phenotypic plasticity as a state-dependent
life-history decision. Evolutionary Ecology 1992, 6(3):243-253.
7. Ricklefs RE, Latham RE: Intercontinental correlation of geographical
ranges suggests stasis in ecological traits of relict genera of temperate
perennial herbs. American Naturalist 1992, 139(6):1305-1321.
8. Peterson AT, Soberón J, Sánchez-Cordero V: Conservatism of ecological
niches in evolutionary time. Science 1999, 285:1265-1267.
9. Prinzing A, Durka W, Klotz S, Brandl R: The niche of higher plants:
evidence for phylogenetic conservatism. Proceedings of The Royal Society
of London Series B-Biological Sciences 2001, 268(1483):2383-2389.
10. Bohning-Gaese K, Schuda MD, Helbig AJ: Weak phylogenetic effects on
ecological niches of Sylvia warblers. Journal of Evolutionary Biology 2003,
16(5):956-965.
11. Losos JB, Jackman TR, Larson A, de Queiroz K, Rodriguez-Schettino L:
Contingency and determinism in replicated adaptive radiations of island
lizards. Science 1998, 279(5359):2115-2118.
12. Graham CH, Ron SR, Santos JC, Schneider CJ, Moritz C: Integrating
phylogenetics and environmental niche models to explore
speciation mechanisms in dendrobatid frogs. Evolution 2004,
58(8):1781-1793.
13. Wiens JJ, Graham CH: Niche conservatism: Integrating evolution, ecology,
and conservation biology. Annual Review of Ecology Evolution and
Systematics 2005, 36:519-539.
14. Linder HP: The radiation of the Cape flora, southern Africa. Biological
Reviews 2003, 78:597-638.
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
15. Parmesan C: Ecological and evolutionary responses to recent climate
change. Annual Review of Ecology and Systematics 2006, 37:637-669.
16. Bradshaw WE, Holzapfel CM: Genetic response to rapid climate change:
it’s seasonal timing that matters. Molecular Ecology 2008, 17:157-166.
17. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J: Climate change and
evolution: disentangling environmental and genetic responses. Molecular
Ecology 2008, 17:167-178.
18. Bennett KJ: Evolution and Ecology: The Pace of Life. Cambridge:
Cambridge University Press; 1997.
19. Coope GR: The response of insect faunas to glacial-interglacial climatic
fluctuations. Philosophical Transactions of the Royal Society of London B
1994, 344:19-26.
20. Huntley B: How plants respond to climate change: migration rates,
individualism and the consequences for plant communities. Annals of
Botany 1991, 67:15-22.
21. Martínez-Meyer E, Peterson AT: Conservatism of ecological niche
characteristics in North American plant species over the Pleistocene-toRecent transition. Global Ecology and Biogeography 2006, 13(4):305-314.
22. Martínez-Meyer E, Peterson AT, Hargrove WW: Ecological niches as stable
distributional constraints on mammal species, with implications for
Pleistocene extinctions and climate change projections for biodiversity.
Global Ecology and Biogeography 2004, 13(4):305-314.
23. McElwain JC, Popa ME, Hesselbo SP, Haworth M, Surlyk F: Macroecological
responses of terrestial vegetation to climatic and atmospheric change
across the Triassic/Jurassic boundary in East Greenland. Paleobiology
2007, 33(4):547-573.
24. McElwain JC, Punyasena SW: Mass extinction events and the plant fossil
record. Trends in Ecology and Evolution 2007, 22(10):548-557.
25. Goldblatt P, Manning J: Cape plants - a conspectus of the Cape flora of
South Africa. Missouri: National Botanical Institute of South Africa and
Missouri Botanical Garden; 2000, 229-230.
26. Zachos J, Pagani M, Sloan L, Thomas E, Billups K: Trends, rhythms, and
aberrations in global climate 65 Ma to present. Science 2001, 292:686-693.
27. Cowling RM, Proches S, Partridge TC: Explaining the uniqueness of the
Cape flora: incorporating geomorphic evolution as a factor for explaining
its diversification. Molecular Phylogenetics and Evolution 2009, 51:64-79.
28. Chase BM, Meadows ME: Late Quaternary dynamics of southern Africa’s
winter rainfall zone. Earth-Science Reviews 2007, 84:103-138.
29. Cowling RM, Cartwright CR, Parkington JE, Allsopp JC: Fossil wood
charcoal assemblages from Elands Bay Cave, South Africa: implications
for Late Quaternary vegetation and climates in the winter-rainfall fynbos
biome. Journal of Biogeography 1999, 26(2):367-378.
30. Deacon J, Lancaster N: Late Quaternary Palaeoenvironments of Southern
Africa. Oxford: Clarendon Press; 1988.
31. Gasse F, Chalie F, Vincens A, Williams MAJ, Williamson D: Climatic patterns
in equatorial and southern Africa from 30,000 to 10,000 years ago
reconstructed from terrestrial and near-shore proxy data. Quaternary
Science Reviews 2008, 27(25-26):2316-2340.
32. Partridge TC, Scott L, Hamilton JE: Synthetic reconstructions of southern
African environments during the Last Glacial Maximum (21-18 kyr) and
the Holocene Altithermal (8-6 kyr). Quaternary International 1999, 5758:207-214.
33. Scott L: Palynological evidence for Late Quaternary warming episodes in
southern Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 1993,
101:229-235.
34. Shi N, Dupont LM, Beug HJ, Schneider R: Vegetation and climate changes
during the last 21000 years in SW Africa based on a marine pollen
record. Vegetation History and Archaeobotany 1998, 7(3):127-140.
35. Johnson SD: Climatic and phylogenetic determinants of flowering
seasonality in the Cape flora. Journal of Ecology 1992, 81:567-572.
36. Bakker FT, Culham A, Hettiarachi P, Touloumenidou T, Gibby M: Phylogeny
of Pelargonium (Geraniaceae) based on DNA sequences from three
genomes. Taxon 2004, 53(1):17-28.
37. Bellstedt DU, van Zyl L, Marais EM, Bytebier B, de Villiers CA, Makwarela AM,
Dreyer LL: Phylogenetic relationships, character evolution and
biogeography of southern African members of Zygophyllum
(Zygophyllaceae) based on three plastid regions. Molecular Phylogenetics
and Evolution 2008, 47:932-949.
38. Bytebier B, Bellstedt DU, Linder HP: A molecular phylogeny for the large
African orchid genus Disa. Molecular Phylogenetics and Evolution 2007,
43(1):75-90.
Page 10 of 11
39. Edwards D, Hawkins JA: Are Cape floral clades the same age?
Contemporaneous origins of two lineages in the genistoids s.l.
(Fabaceae). Molecular Phylogenetics and Evolution 2007, 43:952-970.
40. Forest F, Nanni I, Chase MW, Crane PR, Hawkins JA: Diversification of a
large genus in a continental biodiversity hotspot: temporal and spatial
origin of Muraltia (Polygalaceae) in the Cape of South Africa. Molecular
Phylogenetics and Evolution 2007, 43(1):60-74.
41. Galley C, Linder HP: The phylogeny of the Pentaschistis clade
(Danthonioideae, Poaceae) based on cpDNA, and the evolution and loss
of complex characters. Evolution 2007, 61(4):864-884.
42. Goldblatt P, Savolainen V, Porteous O, Sostaric I, Powell M, Reeves G,
Manning JC, Barraclough TG, Chase MW: Radiation in the Cape flora and
the phylogeny of peacock irises Moraea (Iridaceae) based on four
plastid DNA regions. Molecular Phylogenetics and Evolution 2002,
25:341-360.
43. Hardy CR, Linder HP, Moline P: A phylogeny for the African Restionaceae
and new perspectives on morphology’s role in generating complete
species-phylogenies for large clades. International Journal of Plant Sciences
2008, 169:377-381.
44. Muasya AM, Simpson DA, Verboom GA, Goetghebeur P, Naczi RFC,
Chase MW, Smets E: Phylogeny of Cyperaceae based on DNA sequence
data: current progress and future prospects. Botanical Review 2009, 75:2-21.
45. Mummenhoff K, Al-Shehbaz IA, Bakker FT, Linder HP, Mühlhausen A:
Phylogeny, morphological evolution, and speciation of endemic
Brassicaceae genera in the Cape flora of southern Africa. Annals of the
Missouri Botanical Garden 2005, 92:400-424.
46. Quint M, Classen-Bockhoff R: Phylogeny of Bruniaceae based on matK
and ITS sequence data. International Journal of Plant Sciences 2006,
167(1):135-146.
47. Richardson JE, Welts FM, Fay MF, Cronk QCB, Linder HP, Reeves G,
Chase MW: Rapid and recent origin of species richness in the Cape flora
of South Africa. Nature 2001, 412:181-183.
48. Schrire BD, Lavin M, Barker NP, Cortes-Burns H, von Senger I, Kim JH:
Towards a phylogeny of Indigofera (Leguminosae-Papilionoideae):
identification of major clades and relative ages. In Higher Level
Systematics. Volume 10. Edited by: Klitgaard BB, Bruneau A. Kew: Royal
Botanic Gardens; 2003:269-302.
49. van der Niet T, Johnson SD, Linder HP: Macroevolutionary data suggest a
role for reinforcement in pollination system shifts. Evolution 2006,
60(8):1596-1601.
50. Verboom GA, Linder HP, Stock WD: Phylogenetics of the grass genus
Ehrharta Thunb.: evidence for radiation in the summer-arid zone of the
South African Cape. Evolution 2003, 57:1008-1021.
51. Bakker FT, Culham A, Marais EM, Gibby M: Nested radiation in Cape
Pelargonium. In Plant species-level systematics: new perspectives on pattern
and process. Volume 143. Edited by: Bakker FT, Chatrou LW, Gravendeel B,
Pelser PB. Ruggell, Liechtenstein: A. R. G. Gantner Verlag; 2005:75-100.
52. Boatwright JS, Savolainen V, van Wyk B-E, Schutte-Vlok AL, Forest F, van der
Bank M: Systematic position of the anomalous genus Cadia and the
phylogeny of the tribe Podalyrieae (Fabaceae). Systematic Botany 2008,
33(1):133-147.
53. Galley C, Bytebier B, Bellstedt DU, Linder HP: The Cape element in the
Afrotemperate flora: from Cape to Cairo? Proceedings of the Royal Society
of London Series B 2007, 274:535-543.
54. Linder HP, Hardy CR: Evolution of the species-rich Cape flora. Philosophical
Transactions of the Royal Society B 2004, 359:1623-1632.
55. Quint M, Classen-Bockhoff R: Ancient or recent? Insights into the
temporal evolution of the Bruniaceae. Organisms, Diversity and Evolution
2008, 8:293-304.
56. Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P: Physiological
signals that induce flowering. Plant Cell 1993, 5:1147-1155.
57. Ratchke B, Lacey EP: Phenological patterns of terrestrial plants. Annual
Review of Ecology and Systematics 1985, 16:179-214.
58. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G: Time after
time: flowering phenology and biotic interactions. Trends in Ecology and
Evolution 2007, 22(8):432-439.
59. Levin DA: Flowering phenology in relation to adaptive radiation.
Systematic Botany 2006, 31(2):239-246.
60. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD: Shifting plant
phenology in response to global change. Trends in Ecology and Evolution
2007, 22(7):357-365.
Warren et al. BMC Evolutionary Biology 2011, 11:39
http://www.biomedcentral.com/1471-2148/11/39
61. Fitter AH, Fitter RSR: Rapid changes in flowering time in British plants.
Science 2002, 296:1689-1691.
62. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kubler K,
Bissolli P, Braslavska O, Briede A, et al: European phenological response to
climate change matches the warming pattern. Global Change Biology
2006, 12(10):1969-1976.
63. Dlugosch KM, Parker IM: Invading populations of an ornamental shrub
show rapid life history evolution despite genetic bottlenecks. Ecology
Letters 2008, 11:701-109.
64. Franks SJ, Sim S, Weis AE: Rapid evolution of flowering time by an annual
plant in response to a climate fluctuation. Proceedings of the National
Academy of Sciences of the United States of America 2007, 104:1278-1282.
65. Franks SJ, Weis AE: A change in climate causes rapid evolution of
multiple life-history traits and their interactions in an annual plant.
Journal of Evolutionary Biology 2008, 21:1321-1334.
66. Matsuoka Y, Takumi S, Kawahara T: Flowering time diversification and
dispersal in central Eurasian wild wheat Aegilops tauschii Coss.:
genealogical and ecological framework. PloS ONE 2008, 3(9):e3138.
67. Montague JL, Barrett SCH, Eckert CG: Re-establishment of clinal variation
in flowering time among introduced populations of purple loosestrife
(Lythrum salicaria, Lythraceae). Journal of Evolutionary Biology 2008,
21:234-245.
68. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC: Phylogenetic
patterns of species loss in Thoreau’s woods are driven by climate
change. Proceedings of the National Academy of Sciences of the United States
of America 2008, 105(44):17029-17033.
69. Willis CG, Ruhfel BR, Primack RB, Miller-Rushing AJ, Losos JB, Davis CC:
Favorable climate change response explains non-native species’ success
in Thoreau’s woods. Plos One 2010, 5(1).
70. Stock WD, van der Heyden F, Lewis OAM: Plant structure and function. In
The Ecology of Fynbos: Nutrients, Fire and Diversity. Edited by: Cowling R.
Cape Town: Oxford University Press; 1992:226-240.
71. Proches S, Cowling RM, Du Preez DR: Patterns of geophyte diversity and
storage organ size in the winter-rainfall region of southern Africa.
Diversity and Distributions 2006, 11:101-109.
72. Proches S, Cowling RM, Goldblatt P, Manning JC, Snijman DA: An overview
of the Cape geophytes. Botanical Journal of the Linnean Society 2006,
87:27-43.
73. Van Rooyen MW: Functional aspects of short-lived plants. In The Karoo:
Ecological patterns and processes. Edited by: Dean WRJ, Milton SJ.
Cambridge University Press; 1999.
74. Wolfe JA: Relations of environmental change to angiosperm evolution
during the late Cretaceous and Tertiary. In Evolution and diversification of
land plants. Edited by: Iwatsuki K, Raven PH. New York: Springer;
1997:269-290.
75. Knoll AH, Niklas KJ: Adaptation, plant evolution, and the fossil record.
Review of Palaeobotany and Palynology 1987, 50:127-149.
76. Peterson AT, Tian H, Martínez-Meyer E, Soberón J, Sánchez-Cordero V,
Huntley B: Modeling distributional shifts of individual species and
biomes. In Climate change and biodiversity. Edited by: Lovejoy TE, Hannah L.
New Haven, CT: Yale University Press; 2005:211-228.
77. Peterson AT, Vieglais DA: Predicting species invasions using ecological
niche modeling: new approaches from bioinformatics attack a pressing
problem. Bioscience 2001, 51(5):363-371.
78. Hewitt GM: Some genetic consequences of ice ages, and their role in
divergence and speciation. Biological Journal of the Linnean Society 1996,
58:247-276.
79. Hewitt G: The genetic legacy of the Quaternary ice ages. Nature 2000,
405:907-913.
80. Davis MB, Shaw RG: Range shifts and adaptive responses to Quaternary
climate change. Science 2001, 292:673-679.
81. Davis MD, Shaw RG, Etterson JR: Evolutionary responses to changing
climate. Ecology 2005, 86(7):1704-1714.
82. Maddison WP, Maddison DR: Mesquite: a modular system for
evolutionary analysis. 2006, Version 1.11.
83. Schluter D, Price T, Mooers AØ, Ludwig D: Likelihood of ancestor states in
adaptive radiation. Evolution 1997, 51(6):1699-1711.
84. Cowling RM, Holmes PM: Flora and vegetation. In The Ecology of Fynbos:
Nutrients, Fire and Diversity. Edited by: Cowling RM. Cape Town: Oxford
University Press; 1992:23-61.
Page 11 of 11
85. Schrire BD, Lavin M, Barker NP, Forest F: Phylogeny of the tribe
Indigofereae (Leguminosae-Papilionoideae): geographically structured
more in succulent-rich and temperate settings than in grass-rich
environments. American Journal of Botany 2009, 96:816-852.
doi:10.1186/1471-2148-11-39
Cite this article as: Warren et al.: Consistent phenological shifts in the
making of a biodiversity hotspot: the Cape flora. BMC Evolutionary
Biology 2011 11:39.
Submit your next manuscript to BioMed Central
and take full advantage of:
• Convenient online submission
• Thorough peer review
• No space constraints or color figure charges
• Immediate publication on acceptance
• Inclusion in PubMed, CAS, Scopus and Google Scholar
• Research which is freely available for redistribution
Submit your manuscript at
www.biomedcentral.com/submit